Host ecotype generates evolutionary and epidemiological divergence across a pathogen metapopulation

Abstract

The extent and speed at which pathogens adapt to host resistance varies considerably. This presents a challenge for predicting when-and wherepathogen evolution may occur. While gene flow and spatially heterogeneous environments are recognized to be critical for the evolutionary potential of pathogen populations, we lack an understanding of how the two jointly shape coevolutionary trajectories between hosts and pathogens. The rust pathogen Melampsora lini infects two ecotypes of its host plant Linum marginale that occur in close proximity yet in distinct populations and habitats. In this study, we found that within-population epidemics were different between the two habitats. We then tested for pathogen local adaptation at host population and ecotype level in a reciprocal inoculation study. Even after controlling for the effect of spatial structure on infection outcome, we found strong evidence of pathogen adaptation at the host ecotype level. Moreover, sequence analysis of two pathogen infectivity loci revealed strong genetic differentiation by host ecotype but not by distance. Hence, environmental variation can be a key determinant of pathogen population genetic structure and coevolutionary dynamics and can generate strong asymmetry in infection risks through space.

Understanding the ecology and evolution of host–parasite interactions across scales

“…Jointly, these results demonstrate how landscape configuration may generate variation in evolutionary trajectories among populations, in addition to divergence driven by variation in the abiotic and biotic environment (Wolinska and King ; Laine et al. ).…”

“…In the interaction between L. marginale and M. lini , host ecotypes growing in different habitats yet in close proximity also selected for among population variation in the parasite (Laine et al. ). Much of this among habitat variation is thought to be maintained by differences in soil moisture and microbiota (Tack et al.…”

Durable Resistance of Crops to Disease: A Darwinian Perspective

“…These predictions relate to large populations. Subdivision of populations and environmental variation have significant (83,128,133,135), as does limited population size (134), but how they relate to the durability of RES genes in agriculture is not yet understood.…”

“…Long-lived parasite reproductive structures may also stabilize polymorphism (26). Host and parasite life cycles can be uncoupled in space if different subpopulations of the host and pathogen experience different environmental conditions and if there is gene flow between them (83,128,133,135). The constant turnover of RES and AVR alleles resulting from unstable polymorphism is known as an arms race (56) or the Red Queen Effect.…”

The role of evolutionary biology in research and control of liver flukes in Southeast Asia

“…Finally, a refined understanding of gene flow patterns across the host spectrum as well as of host-parasite demographic processes in a metapopulation context is needed (Thrall and Burdon, 2002; Gandon and Nuismer, 2009; Laine et al, 2014). Greater understanding of gene flow in association with landscape connectivity assessment at different spatial scales can help (1) better characterizing host-parasite local adaptations and geographic co-evolutionary trends, ultimately improving our understanding of virulence, and disease hot spots and (2) infer past and present host and parasite population demographics, including host population expansions and bottlenecks in relation to major landscape/environmental changes, which could in turn help identify which human activities are most likely to foster host population spread or constriction.…”